Specialist and Generalist Fungal Parasites Induce Distinct Biochemical Changes in the Mandible Muscles of Their Host.

Shanshan Zheng,Philip Smith,Liande Wang,David Hughes,Andrew Patterson,Raquel Loreto

doi:10.3390/ijms20184589

Abstract

Some parasites have evolved the ability to adaptively manipulate host behavior. One notable example is the fungus Ophiocordyceps unilateralis sensu lato, which has evolved the ability to alter the behavior of ants in ways that enable fungal transmission and lifecycle completion. Because host mandibles are affected by the fungi, we focused on understanding changes in the metabolites of muscles during behavioral modification. We used High-Performance Liquid Chromatography-Mass/Mass (HPLC-MS/MS) to detect the metabolite difference between controls and O. unilateralis-infected ants. There was a significant difference between the global metabolome of O. unilateralis-infected ants and healthy ants, while there was no significant difference between the Beauveria bassiana treatment ants group compared to the healthy ants. A total of 31 and 16 of metabolites were putatively identified from comparisons of healthy ants with O. unilateralis-infected ants and comparisons of B. bassiana with O. unilateralis-infected samples, respectively. This result indicates that the concentrations of sugars, purines, ergothioneine, and hypoxanthine were significantly increased in O. unilateralis-infected ants in comparison to healthy ants and B. bassiana-infected ants. This study provides a comprehensive metabolic approach for understanding the interactions, at the level of host muscles, between healthy ants and fungal parasites.

Highlights

Some parasites have evolved to manipulate the biting behavior of their insect’s hosts, causing infected individuals to affix themselves by their mandibles to vegetation [1]
We found a significant difference between the global metabolome of O. unilateralis-infected ants and healthy ants, while there was no significant difference between the B. bassiana-treatment ants group compared to the healthy ants
The principal component analysis (PCA) showed that muscles of ants infected by O. unilateralis were markedly different from the muscles of either the positive controls or healthy ants (Figure 1A,B)

Summary

Introduction

Some parasites have evolved to manipulate the biting behavior of their insect’s hosts, causing infected individuals to affix themselves by their mandibles to vegetation [1]. A notable example of this is the behavior changes in ants when infected by species of fungi Ophiocordyceps unilateralis sensu lato (s.l.) [2,3]. Fungi species in this group have evolved to control the biting behavior of ants before death, an adaptive function for the fungus because it removes the infected individual from the ant colony where its development is prevented by the cleaning behavior of the resident ant [4]. Previous morphological studies on this host–parasite system revealed that the muscle fibers of the head experience significant atrophy concomitant with fungal infection [5,6]. Transcriptomics is an important tool that provides insights into the control of insect tissues by fungal pathogens, an additional level of detail could be achieved by analyzing the changes in chemicals directly using a metabolomics approach

Methods

Results

Discussion

Conclusion